Cited by 1,358Insect Resistance and GeneticsInsect-Plant Interactions and ControlInsect Pest Control Strategies

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Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol

Mao, Ying-Bo, Cai, Wen-Juan, Wang, Jia-Wei, Hong, Gao-Jie, Tao, Xiao-Yuan, Wang, Ling-Jian, Huang, Yong-Ping, Chen, Xiao-Ya·2007·Nature Biotechnology

DOI 10.1038/nbt1352

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Abstract

We identify a cytochrome P450 gene (CYP6AE14) from cotton bollworm (Helicoverpa armigera), which permits this herbivore to tolerate otherwise inhibitory concentrations of the cotton metabolite, gossypol. CYP6AE14 is highly expressed in the midgut and its expression correlates with larval growth when gossypol is included in the diet. When larvae are fed plant material expressing double-stranded RNA (dsRNA) specific to CYP6AE14, levels of this transcript in the midgut decrease and larval growth is retarded. Both effects are more dramatic in the presence of gossypol. As a glutathione-S-transferase gene (GST1) is silenced in GST1 dsRNA-expressing plants, feeding insects plant material expressing dsRNA may be a general strategy to trigger RNA interference and could find applications in entomological research and field control of insect pests.

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BackgroundInfluential
Advanced Technologies for Managing Insect Pests
Ishaaya, I., Palli, S. R., & Horowitz, A. R. (2012) · Springer eBooks · doi:10.1007/978-94-007-4497-4 · Cited by 119
Plant-mediated RNAi of a gap gene-enhanced tobacco tolerance against the Myzus persicae
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“The accumulation of siRNAs following the introduction of dsRNAs or from virus infection, has been shown in other insect orders including the Lepidopteran species Helicoverpa armigera [23,24], Spodoptera litura [34] and Bombyx mori [35], and in the Dipteran species Aedes aegypyti [36].”
Background
A Systematic Study of RNAi Effects and dsRNA Stability in Tribolium castaneum and Acyrthosiphon pisum, Following Injection and Ingestion of Analogous dsRNAs
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New Frontiers in Pest Control: Chitosan Nanoparticles-Shielded dsRNA as an Effective Topical RNAi Spray for Gram Podborer Biocontrol
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RNAi-based pest control: Production, application and the fate of dsRNA
He, L., Huang, Y., & Tang, X. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1080576 · Cited by 119
“Silencing the plant Dicer-like enables the accumulation of long dsRNAs, resulting in an enhanced plant-mediated RNAi efficiency in Helicoverpa armigera and Manduca sexta (Mao et al., 2007; Kumar et al., 2012).”
Background
Silencing of an aphid carboxylesterase gene by use of plant-mediated RNAi impairs Sitobion avenae tolerance of Phoxim insecticides
Xu, L., Duan, X., Lv, Y., et al. (2013) · Transgenic Research · doi:10.1007/s11248-013-9765-9 · Cited by 116
“Farmers also face an ever-present threat of insecticide resistance, which leads to a continual search for alternative pest-control strategies (Mao et al. 2007; Baum et al. 2007).”
BackgroundInfluential
Microbial biopesticides: opportunities and challenges.
Koul, O. (2012) · CABI Reviews · doi:10.1079/pavsnnr20116056 · Cited by 116
The function of small RNAs in plant biotic stress response
Huang, J., Yang, M., & Zhang, X. (2016) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12463 · Cited by 118
“Studies on the moth cotton bollworm (Helicoverpa armigera) revealed that plants expressing CYP6AE14 dsRNAs triggered RNAi in the moth midgut, which suppressed the expression of CYP6AE14 and retarded larval growth (Mao et al. 2007; Mao et al. 2011).”
RNAi ‐based gene silencing through dsRNA injection or ingestion against the African sweet potato weevil Cylas puncticollis (Coleoptera: Brentidae)
Prentice, K., Christiaens, O., Pertry, I., et al. (2016) · Pest Management Science · doi:10.1002/ps.4337 · Cited by 116
Physiological and Cellular Responses Caused by RNAi- Mediated Suppression of Snf7 Orthologue in Western Corn Rootworm (Diabrotica virgifera virgifera) Larvae
Ramaseshadri, P., Segers, G. C., Flannagan, R. S., Wiggins, E., Clinton, W. P., Ilagan, O. M., McNulty, B. C., Clark, T. L., & Bolognesi, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054270 · Cited by 115
“In the recent decade, RNAi has been gaining momentum as a biotechnological tool for insect control [1,2,3].”
Background
Towards an understanding of the molecular basis of effective RNAi against a global insect pest, the whitefly Bemisia tabaci
Luo, Y., Chen, Q., Luan, J., Chung, S. H., Eck, J. M. V., Turgeon, R., & Douglas, A. E. (2017) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2017.07.005 · Cited by 114
“…plant protection against the western corn rootworm Diabrotica virgifera virgifera (Baum et al., 2007), cotton bollworm Helicoverpa armigera (Mao et al., 2007) and Colorado potato beetle Leptinotarsa decemlineata (Zhang et al., 2015), and insecticidal RNAi in transgenic crops are reported…”
Background
Oral Delivery Mediated RNA Interference of a Carboxylesterase Gene Results in Reduced Resistance to Organophosphorus Insecticides in the Cotton Aphid, Aphis gossypii Glover
Gong, Y., Yu, X.-R., Shang, Q., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102823 · Cited by 112
Insect pest management in the age of synthetic biology
Fernández, R. M., Petek, M., Gerasymenko, I. M., Juteršek, M., Baebler, Š., Kallam, K., Giménez, E. M., Gondolf, J., Nordmann, A., Gruden, K., et al. (2021) · Plant Biotechnology Journal · doi:10.1111/pbi.13685 · Cited by 112
“The ﬁrst applications of RNAi technology to agricultural pest control were published over a decade ago (Baum et al ., 2007; Mao et al ., 2007).”
Silencing the ecdysone synthesis and signaling pathway genes disrupts nymphal development in the whitefly
Luan, J., Ghanim, M., Liu, S., & Czosnek, H. H. (2013) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2013.05.012 · Cited by 111
Suppressing the activity of trehalase with validamycin disrupts the trehalose and chitin biosynthesis pathways in the rice brown planthopper, Nilaparvata lugens
Tang, B., Yang, M., Shen, Q., et al. (2016) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2016.10.003 · Cited by 111
Key Mechanistic Principles and Considerations Concerning RNA Interference
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“Some kind of RNA silencing pathway (Figure 1A) exists in almost every eukaryotic organism with some notable exceptions among fungi and protists (Nakayashiki et al., 2006; Matveyev et al., 2017).”
Background
Validation of RNA interference in western corn rootworm Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) adults
Rangasamy, M., & Siegfried, B. D. (2011) · Pest Management Science · doi:10.1002/ps.2301 · Cited by 109
Oral Delivery of Double-Stranded RNA in Larvae of the Yellow Fever Mosquito,Aedes aegypti:Implications for Pest Mosquito Control
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Delivery of chitosan/dsRNA nanoparticles for silencing of wing development vestigial ( vg ) gene in Aedes aegypti mosquitoes
kumar, D. R., Kumar, P. S., Gandhi, M. R., Al-Dhabi, N. A., Paulraj, M. G., & Savarimuthu Ignacimuthu, S. J. (2016) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2016.01.030 · Cited by 114
Disruption of Spodoptera exigua larval development by silencing chitin synthase gene A with RNA interference
Chen, X., Tian, H., Zou, L., et al. (2008) · Bulletin of Entomological Research · doi:10.1017/s0007485308005932 · Cited by 109
“Recently, transgenic plants engineered to express insect dsRNAs were reported for entomological research and the field control of insect pests (Baum et al., 2007; Mao et al., 2007).”
Background
Recent insights into cotton functional genomics: progress and future perspectives
Ashraf, J., Zuo, D., Wang, Q., Malik, W., Zhang, Y., Abid, M. A., Cheng, H., Yang, Q., & Song, G. (2017) · Plant Biotechnology Journal · doi:10.1111/pbi.12856 · Cited by 109
“For example, expression of a P450 monooxygenase gene (CYP6AE14) is correlated with larval growth and its expression was induced by gossypol (Mao et al., 2007; Mao et al., 2011; Mao et al., 2013).”
Background
Plant-Generated Artificial Small RNAs Mediated Aphid Resistance
Guo, H., Song, X., Wang, G. G., YANG, K. Y., Wang, Y., Niu, L., Chen, X., & Fang, R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097410 · Cited by 112
“demonstrated that dsRNA expressed in planta could result in the silencing of the corresponding gene in chewing herbivores, and it showed the potential of RNAi as a new way to generate insect-resistant crops [18,19].”
Background
The mitogen-activated protein kinase p38 is involved in insect defense against Cry toxins from Bacillus thuringiensis
Cancino-Rodezno, A., Alexander, C., Villaseñor, R., et al. (2009) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2009.12.010 · Cited by 106
“Recently it was reported that delivering of dsRNA by feeding is an efficient way for specific gene silencing in lepidopteran (Mao et al., 2007) and coleopteran species (Baum et al.”
Background
Development of RNAi Methods for Peregrinus maidis, the Corn Planthopper
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“Thus, ingested dsRNA can be insecticidal and careful design of dsRNA constructs can result in species-specific insecticides [17,18].”
Background
Unbiased Transcriptional Comparisons of Generalist and Specialist Herbivores Feeding on Progressively Defenseless Nicotiana attenuata Plants
Govind, G., Mittapalli, O., Griebel, T., Allmann, S., Böcker, S., & Baldwin, I. T. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008735 · Cited by 106
The novel ABC transporter ABCH1 is a potential target for RNAi-based insect pest control and resistance management
Guo, Z., Kang, S., Zhu, X., Xia, J., Wu, Q., Wang, S., Xie, W., & Zhang, Y. (2015) · Scientific Reports · doi:10.1038/srep13728 · Cited by 104
Functional characterization of three trehalase genes regulating the chitin metabolism pathway in rice brown planthopper using RNA interference
Zhao, L., Yang, M., Shen, Q., et al. (2016) · Scientific Reports · doi:10.1038/srep27841 · Cited by 104
Phylogenetic Origin and Diversification of RNAi Pathway Genes in Insects
Dowling, D., Pauli, T., Donath, A., Meusemann, K., Podsiadłowski, L., Petersen, M., Peters, R. S., Mayer, C., Liu, S., Zhou, X. Y., et al. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw281 · Cited by 107
Tissue-dependence and sensitivity of the systemic RNA interference response in the desert locust, Schistocerca gregaria
Wynant, N., Verlinden, H., Breugelmans, B., et al. (2012) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2012.09.004 · Cited by 104
RNA interference in Nilaparvata lugens (Homoptera: Delphacidae) based on dsRNA ingestion
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Transcriptome Responses in Herbivorous Insects Towards Host Plant and Toxin Feeding
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Biosafety research for non-target organism risk assessment of RNAi-based GE plants
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“The use of plant expressed dsRNA to confer resistance to insects was among the earliest non-research applications to be widely considered, together with use for human therapies, and the first demonstration of its effectiveness was reported in 2007 (Baum et al., 2007; Mao et al., 2007).”
Background
Virus-Derived Gene Expression and RNA Interference Vector for Grapevine
Kurth, E. G., Peremyslov, V. V., Prokhnevsky, A. I., Kasschau, K. D., Miller, M., Carrington, J. C., & Dolja, V. V. (2012) · Journal of Virology · doi:10.1128/jvi.00436-12 · Cited by 102
“Previously, transgenetriggered RNAi was used to control plant-parasitic insects (3, 35), nematodes (27), and viruses (24).”
Method
Silencing Abnormal Wing Disc Gene of the Asian Citrus Psyllid, Diaphorina citri Disrupts Adult Wing Development and Increases Nymph Mortality
El‐Shesheny, I., Hajeri, S., EL-HAWARY, I. S., Gowda, S., & Killiny, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065392 · Cited by 104
“RNAi-mediated silencing of some genes of insect pests has been reported in transgenic plants such as transgenic corn expressing V-ATPase A dsRNA against Diabrotica virgifera [44] and cotton expressing dsRNA of CYP6AE14 against Helicoverpa armigera [86] and these strategies, if applied to citrus, will impact the spread…”
Background
Resistance Mechanisms Against Arthropod Herbivores in Cotton and Their Interactions with Natural Enemies
Hagenbucher, S., Olson, D. M., Ruberson, J. R., WÄCKERS, F. L., & Romeis, J. (2013) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2013.809293 · Cited by 98
“A recent study with H. armigera larvae demonstrated a key role of the P450 mono-oxygenase CYP6AE14 in the detoxification of gossypol (Mao et al., 2007).”
BackgroundInfluential

Authors: Mao, Y.-B., Cai, W.-J., Wang, J.-W., Hong, G.-J., Tao, X.-Y., Wang, L.-J., Huang, Y.-P., & Chen, X.-Y.
Affiliations: Chinese Academy of Sciences (CN)
Corresponding author: Chen, Xiao-Ya
ORCID: Mao, Ying-Bo
Wang, Ling-Jian
Chen, Xiao-Ya
Venue: Nature Biotechnology
Publisher: Springer Science and Business Media LLC
Published: 2007-11
Volume: 25
Issue: 11
Pages: 1307-1313
ISSN: 0733-222X (ISSN-L)
1087-0156
1546-1696
DOI: 10.1038/nbt1352
OpenAlex: W2121440246
Cited by: 1,358
References: 50
Citations by year: 2026: 44 · 2025: 76 · 2024: 80 · 2023: 56 · 2022: 111 · 2021: 98 · 2020: 84 · 2019: 87 · 2018: 67 · 2017: 95 · 2016: 92 · 2015: 89 · 2014: 84 · 2013: 77 · 2012: 68
FWCI: 13.10
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Biotechnology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
Life Sciences › Agricultural and Biological Sciences › Plant Science › Insect Pest Control Strategies
Keywords: Helicoverpa armigera, cytochrome P450 monooxygenase, dsRNA feeding, midgut gene expression, larval growth, insect pest control, plant-insect interactions
MeSH terms: Animals, Gossypium, Cytochrome P-450 Enzyme System, Digestion, Drug Resistance, Glutathione Transferase, Gossypol, Larva, Lepidoptera, Molecular Sequence Data, Pest Control, Biological, RNA, Double-Stranded, Nicotiana, Arabidopsis, RNA, Plant, Insect Proteins, Gene Silencing, Plants, Genetically Modified, RNA Interference, RNA, Small Interfering, Cytochrome P-450 Enzyme Inhibitors

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Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol

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